Distinct structural rearrangements of the VSV glycoprotein drive membrane fusion

Journal of Cell Biology - Tập 191 Số 1 - Trang 199-210 - 2010
Sonia Libersou1, Aurélie Albertini1, Malika Ouldali1, Virginie Maury1, Christine Maheu1, Hélène Raux1, Jean‐Christophe Taveau2, Stéphane Roche1, Yves Gaudin1, Jean Lepault1
1Centre de Recherche de Gif, Laboratoire de Virologie Moléculaire et Structurale, CNRS (UMR 2472), INRA (UMR 1153), IFR115, 91198 Gif-sur-Yvette, France 1
2FEI Company, 5600 KA Eindhoven, Netherlands 2

Tóm tắt

The entry of enveloped viruses into cells requires the fusion of viral and cellular membranes, driven by conformational changes in viral glycoproteins. Many studies have shown that fusion involves the cooperative action of a large number of these glycoproteins, but the underlying mechanisms are unknown. We used electron microscopy and tomography to study the low pH–induced fusion reaction catalyzed by vesicular stomatitis virus glycoprotein (G). Pre- and post-fusion crystal structures were observed on virions at high and low pH, respectively. Individual fusion events with liposomes were also visualized. Fusion appears to be driven by two successive structural rearrangements of G at different sites on the virion. Fusion is initiated at the flat base of the particle. Glycoproteins located outside the contact zone between virions and liposomes then reorganize into regular arrays. We suggest that the formation of these arrays, which have been shown to be an intrinsic property of the G ectodomain, induces membrane constraints, achieving the fusion reaction.

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Tài liệu tham khảo

Albertini, 2006, Crystal structure of the rabies virus nucleoprotein-RNA complex, Science., 313, 360, 10.1126/science.1125280

Backovic, 2009, Class III viral membrane fusion proteins, Curr. Opin. Struct. Biol., 19, 189, 10.1016/j.sbi.2009.02.012

Barge, 1993, Vesicular stomatitis virus M protein may be inside the ribonucleocapsid coil, J. Virol., 67, 7246, 10.1128/jvi.67.12.7246-7253.1993

Blumenthal, 1996, Dilation of the influenza hemagglutinin fusion pore revealed by the kinetics of individual cell-cell fusion events, J. Cell Biol., 135, 63, 10.1083/jcb.135.1.63

Brown, 1988, pH-dependent accumulation of the vesicular stomatitis virus glycoprotein at the ends of intact virions, Virology., 167, 625, 10.1016/S0042-6822(88)90126-2

Chernomordik, 2005, Membrane hemifusion: crossing a chasm in two leaps, Cell., 123, 375, 10.1016/j.cell.2005.10.015

Chernomordik, 1995, Lipids in biological membrane fusion, J. Membr. Biol., 146, 1, 10.1007/BF00232676

Chernomordik, 1998, The pathway of membrane fusion catalyzed by influenza hemagglutinin: restriction of lipids, hemifusion, and lipidic fusion pore formation, J. Cell Biol., 140, 1369, 10.1083/jcb.140.6.1369

Clague, 1990, Gating kinetics of pH-activated membrane fusion of vesicular stomatitis virus with cells: stopped-flow measurements by dequenching of octadecylrhodamine fluorescence, Biochemistry., 29, 1303, 10.1021/bi00457a028

Danieli, 1996, Membrane fusion mediated by the influenza virus hemagglutinin requires the concerted action of at least three hemagglutinin trimers, J. Cell Biol., 133, 559, 10.1083/jcb.133.3.559

Durrer, 1995, Photolabeling identifies a putative fusion domain in the envelope glycoprotein of rabies and vesicular stomatitis viruses, J. Biol. Chem., 270, 17575, 10.1074/jbc.270.29.17575

Gaudin, 2000, Rabies virus-induced membrane fusion pathway, J. Cell Biol., 150, 601, 10.1083/jcb.150.3.601

Gaudin, 1993, Low-pH conformational changes of rabies virus glycoprotein and their role in membrane fusion, J. Virol., 67, 1365, 10.1128/jvi.67.3.1365-1372.1993

Gaudin, 1995, Aggregation of VSV M protein is reversible and mediated by nucleation sites: implications for viral assembly, Virology., 206, 28, 10.1016/S0042-6822(95)80016-6

Gaudin, 1999, Mutations in the glycoprotein of viral haemorrhagic septicaemia virus that affect virulence for fish and the pH threshold for membrane fusion, J. Gen. Virol., 80, 1221, 10.1099/0022-1317-80-5-1221

Ge, 2010, Cryo-EM model of the bullet-shaped vesicular stomatitis virus, Science., 327, 689, 10.1126/science.1181766

Gibbons, 2003, Visualization of the target-membrane-inserted fusion protein of Semliki Forest virus by combined electron microscopy and crystallography, Cell., 114, 573, 10.1016/S0092-8674(03)00683-4

Gibbons, 2004, Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus, Nature., 427, 320, 10.1038/nature02239

Green, 2006, Structure of the vesicular stomatitis virus nucleoprotein-RNA complex, Science., 313, 357, 10.1126/science.1126953

Harrison, 2008, Viral membrane fusion, Nat. Struct. Mol. Biol., 15, 690, 10.1038/nsmb.1456

Kemble, 1994, Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion, Cell., 76, 383, 10.1016/0092-8674(94)90344-1

Kielian, 2006, Virus membrane-fusion proteins: more than one way to make a hairpin, Nat. Rev. Microbiol., 4, 67, 10.1038/nrmicro1326

Kozlov, 2002, The protein coat in membrane fusion: lessons from fission, Traffic., 3, 256, 10.1034/j.1600-0854.2002.030403.x

Lamb, 2007, Structural basis of viral invasion: lessons from paramyxovirus F, Curr. Opin. Struct. Biol., 17, 427, 10.1016/j.sbi.2007.08.016

Leikina, 2004, Influenza hemagglutinins outside of the contact zone are necessary for fusion pore expansion, J. Biol. Chem., 279, 26526, 10.1074/jbc.M401883200

Ludwig, 2008, Electron cryomicroscopy reveals different F1+F2 protein States in intact parainfluenza virions, J. Virol., 82, 3775, 10.1128/JVI.02154-07

Lyles, 1990, Dynamic nature of the quaternary structure of the vesicular stomatitis virus envelope glycoprotein, Biochemistry., 29, 2442, 10.1021/bi00462a002

Malinin, 2001, The rate of lipid transfer during fusion depends on the structure of fluorescent lipid probes: a new chain-labeled lipid transfer probe pair, Biochemistry., 40, 8292, 10.1021/bi010570r

Matlin, 1982, Pathway of vesicular stomatitis virus entry leading to infection, J. Mol. Biol., 156, 609, 10.1016/0022-2836(82)90269-8

Nakai, 1968, The fine structure of vesicular stomatitis virus, Virology., 35, 268, 10.1016/0042-6822(68)90267-5

Navaza, 2002, On the fitting of model electron densities into EM reconstructions: a reciprocal-space formulation, Acta Crystallogr. D Biol. Crystallogr., 58, 1820, 10.1107/S0907444902013707

Roche, 2002, Characterization of the equilibrium between the native and fusion-inactive conformation of rabies virus glycoprotein indicates that the fusion complex is made of several trimers, Virology., 297, 128, 10.1006/viro.2002.1429

Roche, 2004, Evidence that rabies virus forms different kinds of fusion machines with different pH thresholds for fusion, J. Virol., 78, 8746, 10.1128/JVI.78.16.8746-8752.2004

Roche, 2006, Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G, Science., 313, 187, 10.1126/science.1127683

Roche, 2007, Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G, Science., 315, 843, 10.1126/science.1135710

Roche, 2008, Structures of vesicular stomatitis virus glycoprotein: membrane fusion revisited, Cell. Mol. Life Sci., 65, 1716, 10.1007/s00018-008-7534-3

Sánchez-San Martín, 2008, A stable prefusion intermediate of the alphavirus fusion protein reveals critical features of class II membrane fusion, Cell Host Microbe., 4, 600, 10.1016/j.chom.2008.10.012

Skehel, 2000, Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin, Annu. Rev. Biochem., 69, 531, 10.1146/annurev.biochem.69.1.531

Stiasny, 2004, Characterization of a membrane-associated trimeric low-pH-induced Form of the class II viral fusion protein E from tick-borne encephalitis virus and its crystallization, J. Virol., 78, 3178, 10.1128/JVI.78.6.3178-3183.2004

Thomas, 1985, Mass and molecular composition of vesicular stomatitis virus: a scanning transmission electron microscopy analysis, J. Virol., 54, 598, 10.1128/jvi.54.2.598-607.1985

van Heel, 1996, A new generation of the IMAGIC image processing system, J. Struct. Biol., 116, 17, 10.1006/jsbi.1996.0004

Weissenhorn, 2007, Virus membrane fusion, FEBS Lett., 581, 2150, 10.1016/j.febslet.2007.01.093

White, 1981, Cell fusion by Semliki Forest, influenza, and vesicular stomatitis viruses, J. Cell Biol., 89, 674, 10.1083/jcb.89.3.674

Zaitseva, 2005, Class II fusion protein of alphaviruses drives membrane fusion through the same pathway as class I proteins, J. Cell Biol., 169, 167, 10.1083/jcb.200412059